Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 3, 2013, Pages

  Fu, Binqing ^a   Li, Xianchang ^b,c   Sun, Rui ^a   Tong, Xianhong ^d   Ling, Bin ^d   Tian, Zhigang ^a   Wei, Haiming ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ANHUI PROVINCIAL HOSPITAL   (China)

Author keywords

Fetomaternal tolerance; Regulatory NK cells

Indexed keywords

CD27 ANTIGEN; CD56 ANTIGEN; GAMMA INTERFERON;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DECIDUA; FEMALE; FETUS; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; LYMPHOCYTE FUNCTION; MOTHER FETUS RELATIONSHIP; NATURAL KILLER CELL; PRIORITY JOURNAL; SPONTANEOUS ABORTION; TH17 CELL;

ABORTION, HABITUAL; ADULT; ANIMALS; ANTIGENS, CD27; ANTIGENS, CD56; CYTOKINES; DECIDUA; FEMALE; FETUS; HUMANS; IMMUNE TOLERANCE; INTERFERON-GAMMA; ISOANTIGENS; KILLER CELLS, NATURAL; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED DBA; MICE, TRANSGENIC; PREGNANCY; PREGNANCY TRIMESTER, FIRST; TH17 CELLS;

EID: 84872538663     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206322110     Document Type: Article

References (63)

1. Sacks GP, Studena K, Sargent K, Redman CW (1998) Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 179(1):80-86. (Pubitemid 28394477)
2. Trowsdale J, Betz AG (2006) Mother's little helpers: Mechanisms of maternal-fetal tolerance. Nat Immunol 7(3):241-246.
3. Stillerman KP, Mattison DR, Giudice LC, Woodruff TJ (2008) Environmental exposures and adverse pregnancy outcomes: A review of the science. Reprod Sci 15(7):631-650.
4. Sargent IL, Borzychowski AM, Redman CW (2006) NK cells and human pregnancy - An inflammatory view. Trends Immunol 27(9):399-404. (Pubitemid 44216188)
5. Karimi K, Arck PC (2010) Keepers of pregnancy in the turnstile of the environment. Brain Behav Immun 24(3):339-347.
6. Piccinni MP, et al. (1998) Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat Med 4(9):1020-1024.
7. Mjösberg J, Berg G, Jenmalm MC, Ernerudh J (2010) FOXP3+ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol Reprod 82(4):698-705.
8. Saito S, et al. (1999) Quantitative analysis of peripheral blood Th0, Th1, Th2 and the Th1:Th2 cell ratio during normal human pregnancy and preeclampsia. Clin Exp Immunol 117(3):550-555. (Pubitemid 29398304)
9. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG (1993) Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 151(9):4562-4573. (Pubitemid 23318510)
10. Makrigiannakis A, et al. (2001) Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nat Immunol 2(11):1018-1024. (Pubitemid 33069496)
11. Xu C, et al. (2000) A critical role for murine complement regulator crry in fetomaternal tolerance. Science 287(5452):498-501.
12. Zhu XY, et al. (2005) Blockade of CD86 signaling facilitates a Th2 bias at the maternalfetal interface and expands peripheral CD4+CD25+ regulatory T cells to rescue abortion-prone fetuses. Biol Reprod 72(2):338-345.
13. Guleria I, et al. (2005) A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 202(2):231-237. (Pubitemid 41043819)
14. Poehlmann TG, et al. (2005) The possible role of the Jak/STAT pathway in lymphocytes at the fetomaternal interface. Chem Immunol Allergy 89:26-35.
15. Ayatollahi M, Geramizadeh B, Samsami A (2005) Transforming growth factor beta-1 influence on fetal allografts during pregnancy. Transplant Proc 37(10):4603-4604. (Pubitemid 43016091)
16. Zhang J, Xiao X, Liu WT, Demirci G, Li XC (2009) Inhibitory receptors of the immune system: Functions and therapeutic implications. Cell Mol Immunol 6(6):407-414.
17. D'Addio F, et al. (2011) The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol 187(9):4530-4541.
18. Kim YJ, Park SJ, Broxmeyer HE (2011) Phagocytosis, a potential mechanism for myeloid-derived suppressor cell regulation of CD8+ T cell function mediated through programmed cell death-1 and programmed cell death-1 ligand interaction. J Immunol 187(5):2291-2301.
19. Blois SM, et al. (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13(12):1450-1457. (Pubitemid 350224248)
20. Munn DH, et al. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281(5380):1191-1193. (Pubitemid 28406294)
21. Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT (2004) Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112(1):38-43. (Pubitemid 38609820)
22. Tilburgs T, et al. (2009) Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J Reprod Immunol 82(2):148-157.
23. Tilburgs T, et al. (2008) Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol 180(8):5737-5745.
24. Quinn KH, Lacoursiere DY, Cui L, Bui J, Parast MM (2011) The unique pathophysiology of early-onset severe preeclampsia: Role of decidual T regulatory cells. J Reprod Immunol 91(1-2):76-82.
25. Karimi K, Blois SM, Arck PC (2008) The upside of natural killers. Nat Med 14(11):1184-1185.
26. Koopman LA, et al. (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 198(8):1201-1212. (Pubitemid 37323385)
27. Moffett A, Loke C (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6(8):584-594. (Pubitemid 44134091)
28. Pearson H (2002) Reproductive immunology: Immunity's pregnant pause. Nature 420(6913):265-266.
29. Moffett-King A (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2(9):656-663.
30. Vacca P, Moretta L, Moretta A, Mingari MC (2011) Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol 32(11):517-523.
31. Tabiasco J, et al. (2006) Human decidual NK cells: Unique phenotype and functional properties-A review. Placenta 27(Suppl A):S34-39.
32. Nakashima A, Shima T, Inada K, Ito M, Saito S (2012) The balance of the immune system between T cells and NK cells in miscarriage. Am J Reprod Immunol 67(4):304-310.
33. Hanna J, et al. (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12(9):1065-1074. (Pubitemid 44353388)
34. Kalkunte SS, et al. (2009) Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 182(7):4085-4092.
35. Mignini F, Traini E, Tomassoni D, Vitali M, Streccioni V (2008) Leucocyte subset redistribution in a human model of physical stress. Clin Exp Hypertens 30(8):720-731.
36. Evans DL, et al. (2008) Selective serotonin reuptake inhibitor and substance P antagonist enhancement of natural killer cell innate immunity in human immunodeficiency virus/acquired immunodeficiency syndrome. Biol Psychiatry 63(9):899-905. (Pubitemid 351458446)
37. Azpiroz A, De Miguel Z, Fano E, Vegas O (2008) Relations between different coping strategies for social stress, tumor development and neuroendocrine and immune activity in male mice. Brain Behav Immun 22(5):690-698. (Pubitemid 351794231)
38. Vossen MT, et al. (2008) CD27 defines phenotypically and functionally different human NK cell subsets. J Immunol 180(6):3739-3745.
39. Fu B, et al. (2011) CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunology 133(3):350-359.
40. Chiossone L, et al. (2009) Maturation of mouse NK cells is a 4-stage developmental program. Blood 113(22):5488-5496.
41. Le Bouteiller P, Piccinni MP (2008) Human NK cells in pregnant uterus: why there? Am J Reprod Immunol 59(5):401-406. (Pubitemid 351524229)
42. McQueen KL, Parham P (2002) Variable receptors controlling activation and inhibition of NK cells. Curr Opin Immunol 14(5):615-621.
43. Manaster I, et al. (2008) Endometrial NK cells are special immature cells that await pregnancy. J Immunol 181(3):1869-1876.
44. Kopcow HD, et al. (2005) Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc Natl Acad Sci USA 102(43):15563-15568. (Pubitemid 41528096)
45. Mingari MC, Ponte M, Cantoni C, Moretta L (1999) Natural killer cells in pregnancy: How do they avoid attacking fetal tissues? Immunologist 7(4):107-111. (Pubitemid 29471627)
46. Yuan X, et al. (2008) A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J Exp Med 205(13):3133-3144.
47. Wang WJ, et al. (2010) The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod 25(10):2591-2596.
48. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27:485-517.
49. Park H, et al. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6(11):1133-1141. (Pubitemid 41541791)
50. - and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34(4):554-565.
51. Zhou R, Wei H, Tian Z (2007) NK3-like NK cells are involved in protective effect of polyinosinic-polycytidylic acid on type 1 diabetes in nonobese diabetic mice. J Immunol 178(4):2141-2147. (Pubitemid 46233411)
52. Vivier E, Spits H, Cupedo T (2009) Interleukin-22-producing innate immune cells: New players in mucosal immunity and tissue repair? Nat Rev Immunol 9(4):229-234.
53. Bilinski MJ, et al. (2008) Uterine NK cells in murine pregnancy. Reprod Biomed Online 16(2):218-226. (Pubitemid 351291968)
54. Murphy SP, Fast LD, Hanna NN, Sharma S (2005) Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 175(6):4084-4090. (Pubitemid 41292072)
55. Ashkar AA, Di Santo JP, Croy BA (2000) Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 192(2):259-270.
56. Aluvihare VR, Kallikourdis M, Betz AG (2004) Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5(3):266-271.
57. Sasaki Y, et al. (2004) Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 10(5):347-353. (Pubitemid 38714366)
58. Blois S, et al. (2005) Intercellular adhesion molecule-1/LFA-1 cross talk is a proximate mediator capable of disrupting immune integration and tolerance mechanism at the feto-maternal interface in murine pregnancies. J Immunol 174(4):1820-1829. (Pubitemid 40223921)
59. Nagamatsu T, Schust DJ (2010) The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod Sci 17(3):209-218.
60. Wang WJ, et al. (2010) Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol 84(2):164-170.
61. Saito S, Nakashima A, Shima T, Ito M (2010) Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 63(6):601-610.
62. Degli-Esposti MA, Smyth MJ (2005) Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5(2):112-124. (Pubitemid 40208901)
63. Kallikourdis M, Andersen KG, Welch KA, Betz AG (2007) Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc Natl Acad Sci USA 104(2):594-599. (Pubitemid 46123070)